Rapid Responses Against Invasive Species on Islands: Lessons from the Introduced Barbary Ground Squirrel Atlantoxerus Getulus in the Canary Islands

Rapid responses against invasive species on islands: lessons from the introduced Barbary ground squirrel Atlantoxerus getulus in the Canary Islands

F ÉLIX M. MEDINA,MARTA L ÓPEZ-DARIAS and J ULIEN C. PIQUET

Abstract Despite efforts to combat invasive species, further increasing (Martín Esquivel et al., ) and the control of measures are still required to prevent their arrival and some of them entails severe financial costs (e.g. Lampropeltis translocation, especially into biodiverse island ecosystems. californiae; Gesplan, ). The archipelago lacks effective Although many governments worldwide have already estab- control, rapid warning procedures for invasive species, or lished protocols to control alien species, the European a legal framework to control movement of invasive species outermost regions have yet to implement fully effective between islands. prevention or rapid response procedures. The numerous The invasive Barbary ground squirrel Atlantoxerus translocations of the invasive Barbary ground squirrel getulus, which is native to Morocco and Algeria, illustrates Atlantoxerus getulus within the Canary Islands illustrate the situation. A pair of squirrels were taken to Fuerteventura this problem. From  to  at least . individuals in  as pets, and by the s the species had colonized per year have been moved from Fuerteventura to other is- most of the island (López-Darias, ). In Spain the species lands. If movements of these medium-sized vertebrates are is now legally considered an invasive species. Its possession, taking place regularly, the number of smaller species trans- commerce and transportation are banned, although it is still ported within the archipelago could potentially be greater. deliberately moved between islands. Here we review avail- We argue that it is essential to implement stricter strategies able data (from the scientific and grey literature, and per- for invasive species control in these remote biodiversity-rich sonal communications with reliable sources) on known islands, including early detection and rapid response, to translocations of the Barbary ground squirrel in the minimize impacts on native biodiversity. Canary Islands, illustrating the lack of mechanisms preventing movement of invasive species within a European Keywords Alien species, Atlantoxerus getulus, Canary archipelago. islands, prevention, rapid response, squirrels From  to  there were at least  confirmed translocations (involving at least  individuals; Table , Fig. )of Many governments have established guiding principles Barbary ground squirrels between islands. An additional  for the best cost-effective approach to counter problems seven sightings, two in , were not confirmed by knowl- posed by invasive species, and some countries have already edgeable individuals. There was no clear temporal pattern of  developed rapid response strategies and early warning de- translocations (Fig. ), although they occurred in three per- – – – tection programmes (FICMNEW, ; DEFRA, ; iods: , and . Most of the   Genovesi et al., ). For the outermost territories of translocations ( . %) were to Gran Canaria, probably Europe, European Regulation No. / on preventing because of its close commercial and touristic links with and managing invasive alien species, establishes that the Fuerteventura. Gran Canaria is a transit nexus for most of ’ implementation of programmes is the responsibility of the archipelago s commercial routes, and well connected Member states. The regulation specifies that the require- (especially by sea) with Fuerteventura and Lanzarote. In ments to control invasive species should be more restrictive addition, Gran Canaria is the most populated island and in the outermost territories, and preventive measures or Fuerteventura is the main touristic island of the eastern rapid response procedures should be adapted to the specific Canaries, which increases the probability of squirrel translo- features of the territories. However, the regulation is only cations from Fuerteventura. Only a small number of trans- being partly enforced in many of these outermost territories. locations have been detected to Lanzarote, even though it  In the Canary Islands the number of invasive species is is the closest island to Fuerteventura ( km distant). Lanzarote’s human population is six times less than that of Gran Canaria and, even though it is well connected to

FÉLIX M. MEDINA (Corresponding author) Servicio de Medio Ambiente, Cabildo Fuerteventura by sea, the ports are mainly resorts, with de La Palma, Avenida Los Indianos 20, 38700 Santa Cruz de La Palma, Canary few resident islanders, and thus the likelihood of transloca- Islands, Spain. E-mail [email protected] tions is lower. MARTA LÓPEZ-DARIAS and JULIEN C. PIQUET Island Ecology and Evolution Considering the strict controls in place at airports, it is Research Group, Instituto de Productos Naturales y Agrobiología, Consejo Superior de Investigaciones Científicas, Tenerife, Canary Islands, Spain most likely that squirrels are moved by sea. As the keeping Received  October . Revision requested  January . of squirrels is illegal, it is unlikely that escapes will be re- Accepted  January . First published online  May . ported by owners to the relevant authorities. On only one

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09 34,782 53(4), 2019, , TABLE 1 All known confirmed and unconfirmed translocations of the Barbary ground squirrel Atlantoxerus getulus from Fuerteventura to elsewhere in the Canary Islands (see ID numbers in https://www.cambridge.org/core Fig. ) during –, with date of detection or capture if known.

Date of Year of detection/ No. of Other –

786 ID introduction capture Location Island individuals information Source

© Confirmed translocations . https://doi.org/10.1017/S0030605318000200 08Fua&FoaItrainldoi:10.1017/S0030605318000200 International Flora & Fauna 2018 1 1996 La Isleta Gran Canaria 1 Euthanized Calabuig (1999) 2 1997 San Fernando de Maspalomas Gran Canaria 1 Euthanized Calabuig (1999)

. IPaddress: 3 1997 Lomo Blanco, Las Palmas de Gran Canaria 1 Euthanized Calabuig (1999) Gran Canaria 4 1997 Telde Gran Canaria 2 Euthanized Calabuig (1999) 5 1997 Cuatro Puertas, Telde Gran Canaria 1 Euthanized Calabuig (1999) 170.106.202.8 6 1997 Las Palmas de Gran Canaria Gran Canaria 1 Euthanized Calabuig (1999) 7 1997 Monte Lentiscal, Tafira Gran Canaria 2 Euthanized Calabuig (1999) 8 1998 Barranco de Guayadeque Gran Canaria 5 Shot or trapped Calabuig (1999)

, on 9 1998 9 Aug. 1998 La Lechuza, Vega de San Mateo Gran Canaria 1 Castrated & kept in Calabuig (1999)

01 Oct2021 at23:53:25 captivity in CRFS Tafira 10 1998 30 Aug. 1998 Cortijo de Pajonales Gran Canaria 1 Shot Calabuig (1999) 11 2006 8 Nov. 2006 El Cable, Arrecife Lanzarote 1 Trapped Authors’ data 12 2006 13 Nov. 2006 El Cable, Arrecife Lanzarote 1 Trapped Authors’ data 13 2007 1 Feb. 2007 Unspecified Gran Canaria 1 Trapped Fundación Neotrópico,

, subjectto theCambridgeCore termsofuse,available at pers. comm. 14 2007 30 Aug. 2007 Unspecified Gran Canaria 1 Trapped Fundación Neotrópico, pers. comm. 15 2007 5 Nov. 2007 Unspecified Gran Canaria 2 Trapped Fundación Neotrópico, pers. comm. 16 2009 17 Apr. 2009 Batería de San Juan, Las Palmas Gran Canaria 1 Trapped Fundación Neotrópico, de Gran Canaria pers. comm. 17 2014 Muelle de Santa Cruz de Tenerife Tenerife 1 Confiscated because il- Fundación Neotrópico, legally transported pers. comm. 18 2014 La Lomada Grande, Garafía La Palma 1 Euthanized Authors’ data 19 2015 2 Aug. 2015 Punta Gaviota, Vecindario Gran Canaria 1 Photographed but Social network never trapped or later announcement naieseiso sad 783 islands on species Invasive seen 20 2015 5 Oct. 2015 El Burrero, Ingenio Gran Canaria 1 Photographed but Social network never trapped or later announcement seen 21 2016 1 Sep. 2016 Punta de Gando, Telde Gran Canaria 1 Trapped & euthanized Authors’ data 22 2016 15 Nov. 2016 Juncalillo del Sur, San Bartolomé Gran Canaria 1 Found as remains A. Padrón, unpubl. de Tirajana data 23 2016 Santa Cruz de Tenerife Tenerife 1 Trapped Fundación Neotrópico, pers. comm. 784 F. M. Medina et al. comm. data & B. Fariña, pers. comm. comm. Source

FIG. 1 The Canary Islands, showing the locations of all confirmed translocations of Barbary ground squirrels Atlantoxerus getulus during –. Numbers correspond to the ID in Table . White numbers represent the total number of

Other information squirrels translocated to each island.

occasion (ID , Table ) was a squirrel confiscated at a port, which demonstrates the laxity of control measures. As all the islands in the archipelago are climatically suitable for

individuals the Barbary ground squirrel (López-Darias et al., ), the invasion of other islands is only a matter of time unless effective procedures are applied. When a squirrel is reported on islands other than Fuerteventura the relevant government body has to take ac- tions that require both financial and human resources not specifically intended for the purpose. As there is no coordi- nated response protocol, each public administration tackles each detected translocation independently. In  La Palma insular government captured an introduced squirrel shortly after its initial sighting, requiring  h of trapping and c. EUR , (ID , Table ). On Gran Canaria, after failed attempts by the island government to capture two squirrels introduced in , external professionals were subcontracted by the regional authorities (at a cost of EUR ,) almost  year after the original sighting. Following  hours of observation,  questionnaires collected from Location Island No. of Date of detection/ capture 201620162016 Los Giles Cuevas Blancas El Confital Gran Canaria Gran Canaria Gran 1 Canaria 1 1 H. López, pers. comm. S. Martín, pers. comm. N. Migraine, pers. 2016 Amagro Gran Canaria 1 G. González, pers. – – – – .) 201620172017 San Mateo Punta Prieta Gran Canaria Tenerife La Graciosa 1 1 1 R. Gallo, pers. comm. S. J. de L. la Rodríguez-Luengo Cruz, unpubl. 2015 2015 2015 2015 introduction

Cont FIG. 2 Number of known, confirmed translocations of Barbary ground squirrels within the Canary Islands per year from  to . Gaps between years indicate that no translocations were Unconfirmed translocations ID Year of Table 1 ( detected.

the local inhabitants,  ha searched and  h of trapping, translocated squirrels. MLD is funded by the Program Agustín de they captured one squirrel (ID , Table ). Betancourt, under the identification Tenerife  (P. INNOVA   The case of the Barbary ground squirrel is only one ex- - ). JCP is funded by a Canary Islands Government PhD fellowship. ample of the permeability of the sea barriers within this archipelago. If larger animals can be translocated between islands (e.g. the mouflon Ovis orientalis; Acevedo- Rodríguez & Medina, ), it is probably relatively easy Author contributions to translocate smaller animal species and plants. The costs All authors contributed equally to this research and article. of removing invasive species in the whole archipelago are unknown (controlling alien invertebrates on La Palma has been estimated to cost . EUR  million per year; García- References Becerra & Medina, ). Removing naturalized invasive

species is more expensive than preventing their introduction ACEVEDO-RODRÍGUEZ,A.&MEDINA, F.M. () Sobre la presencia (Pimentel et al., ). EU Regulation No. / states del muflón (Ovis orientalis Gmelin, ) en la isla de La Palma that no later than January  all nations should have (Archipiélago Canario). Galemys, , –.  fully operational structures for preventing and controlling CALABUIG,P.( ) Informe sobre las actuaciones realizadas para controlar la incipiente población de ardilla moruna the entry of invasive species. However, the implementation (Atlantoxerus getulus) en la isla de Gran Canaria. Unpublished of those rules is delayed in the Canary Islands. report. Área de Medio Ambiente, Cabildo de Gran Canaria, Canary European outermost regions require an early warning Islands, Spain. and rapid response system, as implemented in New DEFRA () The invasive non-native species framework strategy for Zealand, Australia and Hawaii (e.g. Simberloff et al., ), Great Britain. Department for Environment, Food and Rural to prevent further introductions and translocations of spe- Affairs, London, UK. FICMNEW () A National Early Detection and Rapid Response cies already established in other regions. The creation of System for Invasive Plants in the United States. Federal Interagency such a system, involving governments, decision makers, ex- Committee for the Management of Noxious and Exotic Weeds, perts, NGOs, and other appropriate stakeholders (Simpson Washington, DC, USA. et al., ), is a conservation priority for the Canary Islands GARCÍA-BECERRA,R.&MEDINA, F.M. () Impedir la entrada and other biodiverse island territories. In July  a pilot siempre es más económico que controlar o erradicar. Agropalca, , . trial was approved by the Canary Government for an inva- GENOVESI, P., SCALERA, R., BRUNEL, S., ROY,D.&SOLARZ,W.() sive species detection and intervention network (Gobierno Towards an Early Warning and Information System for Invasive de Canarias, ). The information summarized here has Alien Species (IAS) Threatening Biodiversity in Europe. European been shared with the public administration of the various Environment Agency Technical report No. /, Copenhagen, islands and with other stakeholders, to encourage imple- Denmark. GESPLAN () Control of the invasive species Lampropeltis getula mentation of appropriate control mechanisms, and our re- californiae on the island of Gran Canaria. Http://www. commendations have been passed via internal reports and lifelampropeltis.com/images/pdf/D_EN_Informe_Layman__. personal communications to the Canarian authorities, pdf [accessed  January ]. both at insular and regional level. GOBIERNO DE CANARIAS () Orden de  de julio de , por la que Within the Canary Islands there have not yet been any se encomienda a la empresa pública Gestión y Planeamiento Territorial y Medioambiental, S.A. (GESPLAN) el servicio public education campaigns to communicate the problems denominado ‘Red de Detección e Intervención de Especies Exóticas of invasive species. In the case of the Barbary ground squir- Invasoras en Canarias. Experiencia piloto’. Http://www.gobcan.es/ rel the only action taken to prevent its transportation to boc///.html [accessed  January ]. other islands was to place information plaques at airports LÓPEZ-DARIAS,M.() Ecología de una invasión: el caso de la and ports in the s, but these only remained in place ardilla moruna (Atlantoxerus getulus) en la isla de Fuerteventura. for a few years. In addition to detection and intervention, PhD thesis. Estación Biológica de Doñana and Universidad de La Laguna, La Laguna, Spain. a public education programme is required, to inform society LÓPEZ-DARIAS, M., LOBO, J.M. & GOUAT,P.() Predicting about the risks related to invasive species. potential distributions of invasive species: the exotic Barbary ground squirrel in the Canarian archipelago and the west Mediterranean region. Biological Invasions, , –. Acknowledgements MARTÍN ESQUIVEL, J.L., MARRERO GÓMEZ, M.C., ZURITA, N., ARECHAVALETA,M.&IZQUIERDO ZAMORA,I.() Segundo Lorenzo and Ángel M. Mallorquín helped us in the field in La Biodiversidad en gráficas. Especies silvestres de las Islas Canarias. Palma. Aurelio Martín and Juan Luis Rodríguez-Luengo revised a first Consejería de Medio Ambiente y Ordenación Territorial, Gobierno draft and provided useful data. Fundación Neotrópico, Guillermo de Canarias, Spain. Delgado, Salvador de la Cruz, Susana Saavedra, Jeremías Cabrera, PIMENTEL, D., LACH, L., ZUNIGA,R.&MORRISON,D.() Guillermo González, Beatriz Fariña, Nancia Migraine, Sonia Martín, Environmental and economic costs associated with non-indigenous Heriberto López and Ramón Gallo provided information about species in the United States. BioScience, , –.

SIMBERLOFF, D., MARTIN, J.-L., GENOVESI, P., MARIS, V., WARDLE, Biographical sketches D.A., ARONSON, J. et al. () Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution, , F ÉLIX M. MEDINA studies the trophic feeding ecology of feral cats –. and their impacts on native species on islands, and he is interested SIMPSON, A., JARNEVICH, C., MADSEN, J., WESTBROOKS, R., in the effects of introduced species on the conservation of island eco- ’ FOURNIER, C., MEHRHOFF, L. et al. () Invasive species systems. M ARTA L ÓPEZ-DARIAS S research is mainly focused on the information networks: collaboration at multiple scales for ecology, impacts and management of invasive vertebrate species on is- prevention, early detection, and rapid response to invasive alien lands, particularly on the Canary Islands. J ULIEN C. PIQUET’ S re- species. Biodiversity, , –. search is mainly focused on invasive species and their impact on insular biodiversity and ecological and evolutionary processes.